Mitochondria and NMDA receptor-dependent toxicity of berberine sensitizes neurons to glutamate and rotenone injury

PLoS ONE

Volumn 9, Issue 9, 2014, Pages

  Kysenius, Kai ^a   Brunello, Cecilia A ^a   Huttunen, Henri J ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; BERBERINE; CASPASE 3; CYCLOSPORIN A; DIZOCILPINE; GLUTAMIC ACID; MEMANTINE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; ROTENONE; TACROLIMUS; NEUROTOXIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL VIABILITY; CEREBELLUM; CONTROLLED STUDY; DRUG EFFECT; EMBRYO; ENZYME ACTIVATION; EXCITOTOXICITY; FEMALE; GRANULE CELL; HIPPOCAMPUS; HUMAN; HUMAN CELL; IN VITRO STUDY; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; MITOCHONDRION SWELLING; MOUSE; NERVE CELL LESION; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; OXIDATIVE STRESS; RAT; ANIMAL; ANIMAL EMBRYO; CELL CULTURE; DRUG EFFECTS; DRUG INTERACTION; GENETICS; HEK293 CELL LINE; METABOLISM; NERVE CELL; PATHOLOGY; WISTAR RAT;

ANIMALS; BERBERINE; CELLS, CULTURED; DRUG INTERACTIONS; EMBRYO, MAMMALIAN; GLUTAMIC ACID; HEK293 CELLS; HUMANS; MICE; MITOCHONDRIA; NEURONS; NEUROTOXINS; RATS; RATS, WISTAR; RECEPTORS, N-METHYL-D-ASPARTATE; ROTENONE;

EID: 84907000988     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0107129     Document Type: Article

References (72)

1. Danaei G, Finucane MM, Lu Y, Singh GM, Cowan MJ, et al. (2011) National, regional, and global trends in fasting plasma glucose and diabetes prevalence since 1980: systematic analysis of health examination surveys and epidemiological studies with 370 country-years and 2.7 million participants. Lancet 378: 31-40.
2. McGill JB (2012) Pharmacotherapy in type 2 diabetes: a functional schema for drug classification. Curr Diabetes Rev 8: 257-267.
3. Barnes DE, Yaffe K (2011) The projected effect of risk factor reduction on Alzheimer's disease prevalence. Lancet Neurol 10: 819-828.
4. Imanshahidi M, Hosseinzadeh H (2008) Pharmacological and therapeutic effects of Berberis vulgaris and its active constituent, berberine. Phytother Res 22: 999-1012.
5. Derosa G, Maffioli P, Cicero AF (2012) Berberine on metabolic and cardiovascular risk factors: an analysis from preclinical evidences to clinical trials. Expert Opin Biol Ther 12: 1113-1124.
6. Benaissa F, Mohseni-Rad H, Rahimi-Moghaddam P, Mahmoudian M (2009) Berberine reduces the hypoxic-ischemic insult in rat pup brain. Acta Physiol Hung 96: 213-220.
7. Lau CW, Yao XQ, Chen ZY, Ko WH, Huang Y (2001) Cardiovascular actions of berberine. Cardiovasc Drug Rev 19: 234-244.
8. Jantova S, Cipak L, Cernakova M, Kost'alova D (2003) Effect of berberine on proliferation, cell cycle and apoptosis in HeLa and L1210 cells. J Pharm Pharmacol 55: 1143-1149.
9. Asai M, Iwata N, Yoshikawa A, Aizaki Y, Ishiura S, et al. (2007) Berberine alters the processing of Alzheimer's amyloid precursor protein to decrease Abeta secretion. Biochem Biophys Res Commun 352: 498-502.
10. Zhu F, Qian C (2006) Berberine chloride can ameliorate the spatial memory impairment and increase the expression of interleukin-1beta and inducible nitric oxide synthase in the rat model of Alzheimer's disease. BMC Neurosci 7: 78.
11. Turner N, Li JY, Gosby A, To SW, Cheng Z, et al. (2008) Berberine and its more biologically available derivative, dihydroberberine, inhibit mitochondrial respiratory complex I: a mechanism for the action of berberine to activate AMPactivated protein kinase and improve insulin action. Diabetes 57: 1414-1418.
12. Yao J, Kong W, Jiang J (2013) Learning from berberine: Treating chronic diseases through multiple targets. Sci China Life Sci.
13. Durairajan SS, Liu LF, Lu JH, Chen LL, Yuan Q, et al. (2012) Berberine ameliorates beta-amyloid pathology, gliosis, and cognitive impairment in an Alzheimer's disease transgenic mouse model. Neurobiol Aging 33: 2903-2919.
14. Ji HF, Shen L (2011) Berberine: a potential multipotent natural product to combat Alzheimer's disease. Molecules 16: 6732-6740.
15. Jung HA, Min BS, Yokozawa T, Lee JH, Kim YS, et al. (2009) Anti-Alzheimer and antioxidant activities of Coptidis Rhizoma alkaloids. Biol Pharm Bull 32: 1433-1438.
16. Zhou XQ, Zeng XN, Kong H, Sun XL (2008) Neuroprotective effects of berberine on stroke models in vitro and in vivo. Neurosci Lett 447: 31-36.
17. Serafim TL, Oliveira PJ, Sardao VA, Perkins E, Parke D, et al. (2008) Different concentrations of berberine result in distinct cellular localization patterns and cell cycle effects in a melanoma cell line. Cancer Chemother Pharmacol 61: 1007-1018.
18. Bae J, Lee D, Kim YK, Gil M, Lee JY, et al. (2013) Berberine protects 6-hydroxydopamine-induced human dopaminergic neuronal cell death through the induction of heme oxygenase-1. Mol Cells 35: 151-157.
19. Shin KS, Choi HS, Zhao TT, Suh KH, Kwon IH, et al. (2013) Neurotoxic effects of berberine on long-term L-DOPA administration in 6-hydroxydopamine-lesioned rat model of Parkinson's disease. Arch Pharm Res 36: 759-767.
20. Ye M, Fu S, Pi R, He F (2009) Neuropharmacological and pharmacokinetic properties of berberine: a review of recent research. J Pharm Pharmacol 61: 831-837.
21. Wang X, Wang R, Xing D, Su H, Ma C, et al. (2005) Kinetic difference of berberine between hippocampus and plasma in rat after intravenous administration of Coptidis rhizoma extract. Life Sci 77: 3058-3067.
22. Pereira CV, Machado NG, Oliveira PJ (2008) Mechanisms of berberine (natural yellow 18)-induced mitochondrial dysfunction: interaction with the adenine nucleotide translocator. Toxicol Sci 105: 408-417.
23. Godugu C, Patel AR, Doddapaneni R, Somagoni J, Singh M (2014) Approaches to improve the oral bioavailability and effects of novel anticancer drugs berberine and betulinic Acid. PLoS One 9: e89919.
24. Ma BL, Ma YM, Shi R, Wang TM, Zhang N, et al. (2010) Identification of the toxic constituents in Rhizoma Coptidis. J Ethnopharmacol 128: 357-364.
25. Rodriguez-Menchaca A, Ferrer-Villada T, Lara J, Fernandez D, Navarro-Polanco RA, et al. (2006) Block of HERG channels by berberine: mechanisms of voltage- and state-dependence probed with site-directed mutant channels. J Cardiovasc Pharmacol 47: 21-29.
26. Cannillo M, Frea S, Fornengo C, Toso E, Mercurio G, et al. (2013) Berberine behind the thriller of marked symptomatic bradycardia. World J Cardiol 5: 261-264.
27. Zhang Q, Qian Z, Pan L, Li H, Zhu H (2012) Hypoxia-inducible factor 1 mediates the anti-apoptosis of berberine in neurons during hypoxia/ischemia. Acta Physiol Hung 99: 311-323.
28. Nemoto Y, De Camilli P (1999) Recruitment of an alternatively spliced form of synaptojanin 2 to mitochondria by the interaction with the PDZ domain of a mitochondrial outer membrane protein. EMBO J 18: 2991-3006.
29. Vesikansa A, Sakha P, Kuja-Panula J, Molchanova S, Rivera C, et al. (2012) Expression of GluK1c underlies the developmental switch in presynaptic kainate receptor function. Sci Rep 2: 310.
30. Kysenius K, Muggalla P, Matlik K, Arumae U, Huttunen HJ (2012) PCSK9 regulates neuronal apoptosis by adjusting ApoER2 levels and signaling. Cell Mol Life Sci 69: 1903-1916.
31. Abu-Amero KK, Bosley TM (2005) Detection of mitochondrial respiratory dysfunction in circulating lymphocytes using resazurin. Arch Pathol Lab Med 129: 1295-1298.
32. Hwang JM, Kuo HC, Tseng TH, Liu JY, Chu CY (2006) Berberine induces apoptosis through a mitochondria/caspases pathway in human hepatoma cells. Arch Toxicol 80: 62-73.
33. Wang L, Liu L, Shi Y, Cao H, Chaturvedi R, et al. (2012) Berberine induces caspase-independent cell death in colon tumor cells through activation of apoptosis-inducing factor. PLoS One 7: e36418.
34. Yuan J, Yankner BA (2000) Apoptosis in the nervous system. Nature 407: 802-809.
35. Pereira GC, Branco AF, Matos JA, Pereira SL, Parke D, et al. (2007) Mitochondrially targeted effects of berberine [Natural Yellow 18, 5,6-dihydro- 9,10-dimethoxybenzo(g)-1,3-benzodioxolo(5,6-a) quinolizinium] on K1735-M2 mouse melanoma cells: comparison with direct effects on isolated mitochondrial fractions. J Pharmacol Exp Ther 323: 636-649.
36. Hausenloy DJ, Boston-Griffiths EA, Yellon DM (2012) Cyclosporin A and cardioprotection: from investigative tool to therapeutic agent. Br J Pharmacol 165: 1235-1245.
37. Colombo D, Lunardon L, Bellia G (2014) Cyclosporine and Herbal Supplement Interactions. J Toxicol 2014: 145325.
38. Polster BM, Basanez G, Etxebarria A, Hardwick JM, Nicholls DG (2005) Calpain I induces cleavage and release of apoptosis-inducing factor from isolated mitochondria. J Biol Chem 280: 6447-6454.
39. Yu SW, Wang H, Dawson TM, Dawson VL (2003) Poly(ADP-ribose) polymerase-1 and apoptosis inducing factor in neurotoxicity. Neurobiol Dis 14: 303-317.
40. Nicholls DG, Johnson-Cadwell L, Vesce S, Jekabsons M, Yadava N (2007) Bioenergetics of mitochondria in cultured neurons and their role in glutamate excitotoxicity. J Neurosci Res 85: 3206-3212.
41. Nicholls DG (2008) Oxidative stress and energy crises in neuronal dysfunction. Ann N Y Acad Sci 1147: 53-60.
42. Fukui M, Choi HJ, Zhu BT (2012) Rapid generation of mitochondrial superoxide induces mitochondrion-dependent but caspase-independent cell death in hippocampal neuronal cells that morphologically resembles necroptosis. Toxicol Appl Pharmacol 262: 156-166.
43. Volbracht C, van Beek J, Zhu C, Blomgren K, Leist M (2006) Neuroprotective properties of memantine in different in vitro and in vivo models of excitotoxicity. Eur J Neurosci 23: 2611-2622.
44. Schulz JB, Matthews RT, Henshaw DR, Beal MF (1996) Neuroprotective strategies for treatment of lesions produced by mitochondrial toxins: implications for neurodegenerative diseases. Neuroscience 71: 1043-1048.
45. Budd SL, Nicholls DG (1996) Mitochondria, calcium regulation, and acute glutamate excitotoxicity in cultured cerebellar granule cells. J Neurochem 67: 2282-2291.
46. Li CY, Chin TY, Chueh SH (2004) Rat cerebellar granule cells are protected from glutamate-induced excitotoxicity by S-nitrosoglutathione but not glutathione. Am J Physiol Cell Physiol 286: C893-904.
47. Ward MW, Rego AC, Frenguelli BG, Nicholls DG (2000) Mitochondrial membrane potential and glutamate excitotoxicity in cultured cerebellar granule cells. J Neurosci 20: 7208-7219.
48. Wang H, Yu SW, Koh DW, Lew J, Coombs C, et al. (2004) Apoptosis-inducing factor substitutes for caspase executioners in NMDA-triggered excitotoxic neuronal death. J Neurosci 24: 10963-10973.
49. Gomez C, Bandez MJ, Navarro A (2007) Pesticides and impairment of mitochondrial function in relation with the parkinsonian syndrome. Front Biosci 12: 1079-1093.
50. Betarbet R, Sherer TB, MacKenzie G, Garcia-Osuna M, Panov AV, et al. (2000) Chronic systemic pesticide exposure reproduces features of Parkinson's disease. Nat Neurosci 3: 1301-1306.
51. Greenamyre JT, MacKenzie G, Peng TI, Stephans SE (1999) Mitochondrial dysfunction in Parkinson's disease. Biochem Soc Symp 66: 85-97.
52. Isaev NK, Stelmashook EV, Ruscher K, Andreeva NA, Zorov DB (2004) Menadione reduces rotenone-induced cell death in cerebellar granule neurons. Neuroreport 15: 2227-2231.
53. Johnson-Cadwell LI, Jekabsons MB, Wang A, Polster BM, Nicholls DG (2007) 'Mild Uncoupling' does not decrease mitochondrial superoxide levels in cultured cerebellar granule neurons but decreases spare respiratory capacity and increases toxicity to glutamate and oxidative stress. J Neurochem 101: 1619-1631.
54. Chan E (1993) Displacement of bilirubin from albumin by berberine. Biol Neonate 63: 201-208.
55. Linn YC, Lu J, Lim LC, Sun H, Sun J, et al. (2012) Berberine-induced haemolysis revisited: safety of Rhizoma coptidis and Cortex phellodendri in chronic haematological diseases. Phytother Res 26: 682-686.
56. Carlsson CM (2010) Type 2 diabetes mellitus, dyslipidemia, and Alzheimer's disease. J Alzheimers Dis 20: 711-722.
57. Kwon IH, Choi HS, Shin KS, Lee BK, Lee CK, et al. (2010) Effects of berberine on 6-hydroxydopamine-induced neurotoxicity in PC12 cells and a rat model of Parkinson's disease. Neurosci Lett 486: 29-33.
58. Lee T, Heo H, Kim Kwon Y (2010) Effect of Berberine on Cell Survival in the Developing Rat Brain Damaged by MK-801. Exp Neurobiol 19: 140-145.
59. Cui HS, Matsumoto K, Murakami Y, Hori H, Zhao Q, et al. (2009) Berberine exerts neuroprotective actions against in vitro ischemia-induced neuronal cell damage in organotypic hippocampal slice cultures: involvement of B-cell lymphoma 2 phosphorylation suppression. Biol Pharm Bull 32: 79-85.
60. Hsu YY, Chen CS, Wu SN, Jong YJ, Lo YC (2012) Berberine activates Nrf2 nuclear translocation and protects against oxidative damage via a phosphatidylinositol 3-kinase/Akt-dependent mechanism in NSC34 motor neuron-like cells. Eur J Pharm Sci 46: 415-425.
61. Hsu YY, Tseng YT, Lo YC (2013) Berberine, a natural antidiabetes drug, attenuates glucose neurotoxicity and promotes Nrf2-related neurite outgrowth. Toxicol Appl Pharmacol 272: 787-796.
62. Edwards MA, Loxley RA, Williams AJ, Connor M, Phillips JK (2007) Lack of functional expression of NMDA receptors in PC12 cells. Neurotoxicology 28: 876-885.
63. Nicholls DG, Budd SL (2000) Mitochondria and neuronal survival. Physiol Rev 80: 315-360.
64. Mikes V, Dadak V (1983) Berberine derivatives as cationic fluorescent probes for the investigation of the energized state of mitochondria. Biochim Biophys Acta 723: 231-239.
65. Borodina VM, Zelenin AV (1977) [Fluorescence microscopy demonstration of mitochondria in tissue culture cells using berberine]. Tsitologiia 19: 1067-1068.
66. Nunnari J, Suomalainen A (2012) Mitochondria: in sickness and in health. Cell 148: 1145-1159.
67. Wu J, Jin GZ (1997) Tetrahydroberberine blocks membrane K+ channels underlying its inhibition of intracellular message-mediated outward currents in acutely dissociated CA1 neurons from rat hippocampus. Brain Res 775: 214-218.
68. Sanchez-Chapula J (1996) Increase in action potential duration and inhibition of the delayed rectifier outward current IK by berberine in cat ventricular myocytes. Br J Pharmacol 117: 1427-1434.
69. Wang YX, Zheng YM, Zhou XB (1996) Inhibitory effects of berberine on ATPsensitive K+ channels in cardiac myocytes. Eur J Pharmacol 316: 307-315.
70. Yoo KY, Hwang IK, Lim BO, Kang TC, Kim DW, et al. (2006) Berberry extract reduces neuronal damage and N-Methyl-D-aspartate receptor 1 immunoreactivity in the gerbil hippocampus after transient forebrain ischemia. Biol Pharm Bull 29: 623-628.
71. Goldberg I, Auriel E, Russell D, Korczyn AD (2012) Microembolism, silent brain infarcts and dementia. J Neurol Sci 322: 250-253.
72. Tanner CM, Kamel F, Ross GW, Hoppin JA, Goldman SM, et al. (2011) Rotenone, paraquat, and Parkinson's disease. Environ Health Perspect 119: 866-872.